Mental disorders in children and adolescents with lower urinary tract dysfunction

Correspondence to: Eleonora Moreira Lima. Universidade federal de Minas Gerais Faculdade de Ciências Médicas de Minas Gerais. Rua Piauí, no 933, Apt 501, Belo Horizonte, MG, Brazil. CEP: 30150-320 E-mail: eleonoralima@uol. com.br Esse estudo contou com o financiamento da FAPEMIG (projeto número 21557). Também contou com o apoio da PróReitoria de Pós-Graduação da UFMG através do Convênio CAPES/PRPQ/UFMG. Coautor MGFC foi contemplada com bolsa pelo CNPq. IntroductIon


IntroductIon
Lower urinary tract dysfunction (LUTD) is an umbrella term that encompasses a spectrum of disorders affecting bladder filling and/or voiding in the absence of neurologic disease or obstructive uropathy.A lack of consistency in terminology has resulted in a reported prevalence of symptoms of LUTD in children ranging from 2% to 25%. 1,2ccording to the consensus published by the International Children's Continence Society (ICCS), LUTD symptoms are categorized based on whether Lower urinary tract dysfunction (LUTD) affects about 2-25% of the pediatric population and is associated with the presence of emotional and behavioral disorders.The purpose of this literature review was to identify studies focusing on mental disorders in children and adolescents with LUTD.The prevalence of these disorders is high -ranging from about 20 to 40% -in children with symptoms of LUTD and comorbidities.The presence of emotional and behavioral symptoms impact in the treatment of the dysfunction, self-esteem of patients and caregivers.Despite the association between mental/behavioral disorders and LUTD be well documented in the literature, the investigation of psychiatric symptoms in clinical practice is still not common and should be stimulated.

resumo
Palavras-chave: adolescente; criança; enurese noturna; incontinência urinária; transtornos mentais.they are related to bladder filling or voiding.The following are storage symptoms: increased or decreased voiding frequency; incontinence; urinary urgency; nocturia.Voiding symptoms include: hesitancy; straining; weak stream; intermittent stream; urinary retention; feeling of incomplete voiding; postmicturition dribble; dysuria.The comorbidities usually associated with LUTD are urinary tract infection, asymptomatic bacteriuria, constipation, and/or fecal incontinence, vesicoureteral reflux, emotional disorders, and intellectual disability. 3n addition to posing risk to the upper urinary tract, LUTD may cause embarrassment and emotional impact on parents and children due to the frustration inherent to dealing with urinary incontinence.An important association between LUTD and mental disorder has been described in a number of studies.
The prevalence of behavioral disorders in children diagnosed with psychiatric comorbidities is significant: 20-30% of them suffer from nocturnal enuresis; 20-40% have diurnal incontinence; and 30-50% have fecal incontinence. 4,5In children and adolescents from the general population the prevalence of psychiatric disorders is of approximately 10%. 6espite the increased frequency of psychiatric disorders observed in this population, symptoms are usually not targeted in the care delivered to these patients, in what might be categorized as neglect toward children with LUTD in an important area of their lives. 4

objectIve
This study aimed to review the literature on the topic in order to assess the degree of attention paid to behavioral and emotional symptoms in clinical practice as per the ICSS recommendations.

dIscussIon
In the last decade, the relationship between lower urinary tract dysfunction and psychiatric disorder has been extensively studied.According to Franco, 7 the central nervous system (CNS) is involved in the etiology of most cases of pediatric LUTD, switching from a longstanding vesicocentric model to understand the disease into a neurocentric one.Changes in CNS function and anatomy have also been associated with psychiatric disorders.The neurocentric model facilitates the comprehension of the amply documented association between depression, enuresis, and encopresis. 7on Gontard and Equit 8 stressed the association between altered CNS activity and different forms of incontinence and psychiatric disorders such as attention deficit and hyperactivity disorder (ADHD).Areas of the brain such as the insula, the anterior cingulate cortex, and the prefrontal cortex are responsible for bladder control and monitoring 9 and have been implicated in ADHD and LUTD. 8yde et al. 10 considered enuresis during childhood a premorbid developmental marker of schizophrenia.In a group of patients with schizophrenia, 21% had enuresis during childhood versus 11% of their siblings and 7% of healthy controls.Neuroimaging studies revealed global grey matter volume reductions in schizophrenic and non-schizophrenic individuals with a history of enuresis during childhood.
One might infer that, at least in schizophrenic individuals, the anomalous development of the right superior temporal gyrus was associated with enuresis during childhood.Absence of incontinence in later stages of life suggests functional adaptation.According to Franco, 7 these findings support the idea that the frontal lobes are closely involved in the development and maintenance of bladder control.
In another study, adult patients with urinary urgency had increased anterior cingulate cortex activity levels and decreased activity in the orbitofrontal cortex (OFC). 11Yang et al. 12 compared children with ADHD to children with ADHD and enuresis, and observed the latter had shorter response times in neuropsychological tests devised to assess attentional performance, revealing they had less inhibitory control.Understanding this pathophysiological correlation and the importance of treating psychiatric comorbidities are key steps lower urinary tract dysfunction: 56% of the children postponing voiding had clinical-range scores in the CBCL versus 24% of the children with urinary incontinence. 15In a group of preschoolers, Niemczyk et al. 19 saw externalizing disorders in 14.5% of the individuals with monosymptomatic nocturnal enuresis, whereas children with diurnal incontinence and continent children had similar prevalence rates (9.5%).

EnurEsis
Involuntary urination while asleep is called nocturnal enuresis.Children who wet their beds but have no other urinary tract symptoms have monosymptomatic nocturnal enuresis (MNE).Children who urinate on their beds while asleep and have symptoms of lower urinary tract dysfunction are diagnosed with non-monosymptomatic nocturnal enuresis (NMNE). 20ediatric enuresis appears to be strongly associated with attention deficit and hyperactivity disorder (ADHD), as described by Baeyens et al. 21These authors reported a prevalence of 15% of combined ADHD (inattentive/hyperactive) in a population of children with enuresis and 22.5% of predominantly inattentive ADHD, while in the general pediatric population the prevalence of ADHD ranged between 3-5%. 6hreeram et al. 22 looked into the prevalence of enuresis in the United States and found a strong association with ADHD, in which children with enuresis had a 2.88-fold chance of having ADHD when compared to healthy controls.Yang et al. 23 reported that boys with elevated scores for symptoms of ADHD tended to have higher scores for LUTD in the Dysfunctional Voiding Symptom Score (DVSS).The DVSS is a scale used to assess lower urinary tract symptoms in the general population. 24ower urinary tract symptoms correlated with scores in the Swanson, Nolan e Pelham-IV (SNAP-IV), a scale used to assess symptoms of ADHD and ODD. 25 in attaining more promising therapies for patients with LUTD. 7ost of the studies designed to look into the psychiatric symptoms of patients with LUTD were based on the Child Behavior Checklist (CBCL), a questionnaire developed to assess the social skills and behavioral problems of individuals aged 6-18 years. 13lthough the CBCL is not a diagnostic tool, elevated scores in its subscales are highly sensitive and specific in characterizing some mental disorders in children and adolescents.
The CBCL groups behavioral problems into internalizing -the summation of scores related to anxiety/depression, withdrawn-depressed, and somatic complaints -and externalizing -the summation of scores in delinquent behavior and aggressive behavior -problem scales. 14uhn et al. 15 reported superior prevalence of clinical-range scores in the CBCL for children and adolescents with LUTD (41%) when compared to healthy controls (9%).There seems to be a distinct pattern between the occurrence of internalizing and externalizing symptoms in this group of children.The prevalence of the first -depression and anxiety disorder -was 29% in the group with LUTD versus 6% in healthy controls.The prevalence of externalizing problems -conduct disorder and attention deficit and hyperactivity disorder -was 35% versus 0%, respectively. 15hildren with LUTD also had higher rates of depressive, aggressive, and inattentive symptoms. 16he rates of psychiatric comorbidity in a group of 1001 children with bladder and bowel dysfunction were up to six times higher than the rates seen in the general population -43% had clinical-range scores in the CBCL, 36% with externalizing problems and 33% with internalizing problems. 17The same author described higher rates of symptoms of oppositional defiant disorder (ODD) in children with incontinence than in healthy controls (19.5% vs. 5.2%). 18n addition to the elevated prevalence of mental disorders in the population with LUTD, the occurrence of the phenomenon varied depending on the type of Another study found that children with MNE had a 2.5-fold chance of presenting emotional disorders than controls. 26Children with NMNE had even higher scores for behavioral problems when compared to a group of individuals with MNE. 17,26A prospective study enrolling more than 8,000 children, The Avon Longitudinal Study of Parents and Children (ALSPAC) by Joinson et al., 27 reported a positive association between difficult temperament and behavioral problems in early childhood and occurrence of enuresis in school years.

Diurnal EnurEsis
Children with diurnal enuresis seem to be more affected by psychological problems.They had about twice the rate of externalizing disorders than children without diurnal enuresis.The following disorders stood out from the list: ADHD -24.8%;ODD -10.9%; conduct disorder -11.8%.
Twenty-nine percent of the children with diurnal enuresis had internalizing disorders. 28Another large epidemiologic study with approximately 8,000 children found that individuals suffering from diurnal enuresis (10.4%) had more gastrointestinal, urinary, and psychological symptoms than controls. 29Kuhn et al. 15 reported that 49% of the children with diurnal enuresis met the diagnostic criteria for at least one mental disorder described in the International Classification of Diseases -10 th revision (ICD-10).
A study carried out with 138 children diagnosed with urinary incontinence described associations between psychiatric symptoms and worse quality of life (QOL), older age, being non-Caucasian, and female sex.Worsening clinical condition was not associated with decreases in QOL. 30 Joinson et al. 31 looked at predictors for poor sphincter controlurinary and fecal incontinence -and described developmental delays, difficult temperament, and maternal depression and anxiety as risk factors.
Von Gontard et al. 32 estimated that behavioral disorders, oppositional defiant disorder and attention deficit and hyperactivity disorder in particular, were twice as prevalent in individuals with LUTD than in the general population.Another study found that children with diurnal enuresis had 4.4-fold risk of ADHD. 33pact ADHD negatively affects resolution rates of LUTD; children with ADHD had more trouble complying with LUTD therapy and were less responsive to alarm interventions than controls. 34pproximately 65% of the children with enuresis had clinical-range scores in the Child Behavior Checklist (CBCL) and higher rates of social and behavioral problems. 32,35Üçer & Gümüş 36 studied a group of children with monosymptomatic nocturnal enuresis (MNE) and found higher rates of poor quality of life, poor sleep, and depression.
The authors of a prospective study evaluated the presence of psychiatric symptoms before and after LUTD therapy and were unable to find changes in the prevalence of internalizing problems.However, externalizing symptoms and total problems in the CBCL decreased (14% to 7%; and 23% to 8%, respectively) in the group with voiding dysfunction.The behavioral symptoms of the individuals in the group with urinary urgency did not ameliorate significantly. 37reating patients with ADHD and LUTD was more difficult than treating individuals with LUTD alone. 7Baeyens et al. 38 followed a group of patients for two years and reported persistence of enuresis in 72.5% of the patients with ADHD, suggesting that individuals with ADHD had more trouble complying with treatment.Even in cases in which enuresis resolved, ADHD persisted, indicating that the symptoms reflected the existence of a neurodevelopmental disorder independent from enuresis.Therefore, one might infer that ADHD interferes with the treatment and prognosis of enuresis.
However, children offered proper treatment for ADHD and children without ADHD have similar rates of urinary incontinence, implying that the treatment of ADHD might be associated with positive effects on the resolution of incontinence. 39The best mode of treatment for incontinence associated with ADHD appears to be individualized multimodal therapy, which includes behavior modification combined with drug and/or biofeedback therapy and provides for increased effectiveness when compared to monotherapy. 40n a study on stressful events of childhood, nocturnal enuresis was rated as difficult by 36.7% of the children and ranked eighth among stressful life events. 41The stress experienced by many of the children with LUTD was linked to incontinence and subclinical motional symptoms that compromised the treatment and prognosis of LUTD. 4 The impacts of the dysfunction appear to be felt by parents and caregivers alike.De Bruyne et al. 16 reported increased levels of stress in parents of children with LUTD and behavioral disorders.Mothers of children with enuresis had poorer quality of life and more anxiety symptoms than the mothers of controls.Treatment of enuresis led to significant improvements in the QOL of mothers and children. 42Table 1 lists the main quantitative studies published since the year 2000 to address the psychosocial involvements seen in pediatric patients with LUTD.

conclusIon
Pediatric patients with LUTD often present with psychiatric disorders.This evident association reinforces the current idea that the central nervous system is involved in the etiology of most urinary tract disorders affecting children, contrary to the thought that the bladder was solely responsible for these disorders. 7imilarly to enuresis-free children, pediatric patients with MNE had lower emotional comorbidity rates.In the studies included in this review, the pediatric population with diurnal enuresis seems to have been more affected by psychological problems, whereas children with urinary urgency and incontinence showed internalizing symptoms; children postponing micturition -who often suffered from fecal retention, encopresis, and ODD -had higher rates of externalizing disorders. 25Children with diurnal enuresis and fecal incontinence are in greater need for mental health care.The impact of these dysfunctions also appears to spill over and affect parents and caregivers with significant levels of stress. 21t should be noted that most of the studies screened patients with LUTD for psychiatric symptoms, which in itself does not constitute diagnosis; only specialized health care professionals may diagnose the occurrence of psychiatric disorders based on the criteria dictated by the DSM or the ICD.Therefore, whenever symptoms of this nature are present, the patient must be referred to specialized care and treatment. 4iven the high rate of psychiatric comorbidities in children with LUTD, the search for related symptoms gains relevance and is recommended for every child with diurnal enuresis or other symptoms of LUTD or fecal incontinence.Emotional and behavioral disorders compromise compliance with treatment and lead to poorer prognosis.
Therefore, pediatricians and other health care workers recognizing psychiatric disorders in patients with LUTD should refer them to specialized care in order to mitigate their suffering and improve their prognostic chances.Likewise, mental health care workers must be aware of the possible associations between psychiatric disorders and LUTD.